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Parasitic Diseases of Zoonotic Importance in Humans of Northeast India, with Special Reference to Ocular Involvement

Parasitic Diseases of Zoonotic Importance in Humans of Northeast India, with Special Reference to Ocular Involvement

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Open Access Full Text Article Review Parasitic diseases of zoonotic importance in humans of northeast , with special reference to ocular involvement

Dipankar Das1 Abstract: Parasitic zoonotic diseases are prevalent in India, including the northeastern states. Saidul Islam2 Proper epidemiological data are lacking from this part of the country on zoonotic parasitic Harsha Bhattacharjee1 diseases, and newer diseases are emerging in the current scenario. Systemic manifestation Angshuman Deka1 of such diseases as , , hydatidosis, and toxoplasmosis are fairly Dinakumar Yambem1 common. The incidence of acquired toxoplasmal infection is showing an increasing trend Prerana Sushil Tahiliani1 in association with acquired immunodeficiency syndrome. Among the ocular parasitic dis- eases, toxoplasmosis, cysticercosis, , , , hydatidosis, Panna Deka1 amebiasis, giardiasis, etc, are the real problems that are seen in this subset of the population. Pankaj Bhattacharyya1 Therefore, proper coordination between various medical specialities, including veterinary 1 Satyen Deka science and other governing bodies, is needed for better and more effective strategic planning 1 Kalyan Das to control zoonoses. 1 Gayatri Bharali Keywords: zoonoses, regional infections, toxoplasmosis, cysticercosis, toxocariasis, 1 Apurba Deka hydatidosis Rajashree Paul1 1Sri Sankaradeva Nethralaya, Introduction Guwahati, 2Department of Parasitology, College of Veterinary India is the second-most densely inhabited and seventh-largest country in the world, Science, Assam Agricultural University, and there is a lot of variation in the geographic areas, ethnicity, religion, food habits, Guwahati, Assam, India personal behavior, level of education, and standard of living.1 The recent census of the country showed that 72.2% of the population lived in rural areas, with over 70% of this population owning livestock, which play an important role in the causation of zoonotic diseases in humans. Parasitic zoonoses affect human as well as health directly and indirectly, which may affect the socioeconomic condition of the country as a whole. Poor economic conditions, sanitation, water supply, and personal habits are some of the causes on the Indian subcontinent of harboring the zoonoses, particularly in the northeast part of India.1 This paper focuses on important parasitic zoonoses in Assam and other northeastern states of India.

Toxoplasmosis 2 Correspondence: Dipankar Das Toxoplasmosis is a common disease in both mammals and birds. The disease is caused Department of Ocular Pathology, by the obligate intracellular protozoan Toxoplasma gondii. Intermediate hosts include Uveitis and Neuro-Ophthalmology Services, Sri Sankaradeva Nethralaya, sheep, goats, pigs, and humans. Oocysts of T. gondii are uniquely found in the intestinal Beltola, Guwahati, Assam 781028, India mucosa of cats (definitive hosts). Once they are released, they spread to humans and Tel +91 361 222 8879/230 5516 other through a variety of vectors. Toxoplasmosis in the central nervous system Fax +91 361 222 8878 Email [email protected] is nowadays seen in acquired immunodeficiency syndrome (AIDS) patients in India.3

submit your manuscript | www.dovepress.com Eye and Brain 2014:6 1–8 1 Dovepress © 2014 Das et al. This work is published by Dove Medical Press Limited, and licensed under Creative Commons Attribution – Non Commercial (unported, v3.0) License. The full terms of the License are available at http://creativecommons.org/licenses/by-nc/3.0/. Non-commercial uses of the work are permitted without any further http://dx.doi.org/10.2147/EB.S64404 permission from Dove Medical Press Limited, provided the work is properly attributed. Permissions beyond the scope of the License are administered by Dove Medical Press Limited. Information on how to request permission may be found at: http://www.dovepress.com/permissions.php Das et al Dovepress

Serum IgA titers in enzyme-linked immunosorbent assays sign of acquired active toxoplasmosis is a whitish yellow (ELISAs) are positive in chronic toxoplasmosis, whereas IgM retinal lesion associated with hazy vitreous as a result of the is positive in acute infection. Therefore, the titers for both presence of vitreous cells (“headlight in the fog” ­appearance). IgG and IgM are important, and need to be strongly corre- Old retinochoroidal scars can often be seen adjacent to the lated with clinical findings. In a national serological survey new whitish yellow lesion. The areas of retinitis are the in India,4 a total of 23,094 serum samples were tested for result of tissue-cyst bursting and releasing bradyzoites that antibodies to the parasite. IgG and IgM antibodies were found transform into tachyzoites, which in turn invade the neigh- to be positive in 24.3% and 2% of the samples, respectively. boring cells. These destructive lesions are usually larger The lowest seroprevalence value was obtained in north India, than one disk diameter, and appear as soft, white, fluffy while it was highest in the south.4 The data probably indicate infiltrates surrounded by retinal edema with choroiditis.9–11 the effect of significantly drier conditions in the north, leading When the tachyzoites come under increasing attack by the to reduced survivability of T. gondii oocysts. host’s immune response, they gradually transform back into Our previous study,5 conducted in a tertiary eye-care cen- inflammatory exudates, and are frequently present around the ter in one of the northeast states (Assam) of India, showed 37 retinal vessels adjacent to an area of active inflammation. cases of toxoplasmal uveitis (40.21%) in 1 year compared to Chorioretinal scars are occasionally found in uninvolved 27.87% by Biswas et al6 from south India. Out of the 37 cases, areas. Patients often complain of blurred vision, floaters, 14 were acquired, while 23 cases were congenital toxoplasmal photophobia, and pain in the affected eye. Occasionally, retinochoroidal lesions. Serum IgG only was positive in 30 of the initial presentation would be severe unilateral papillitis, 37 cases and IgM only in three cases, while both serum IgG macular hard exudates distributed in star-like fashion, and and IgM positivity was observed in four cases. Chorioretinitis vitreal inflammation simulating neuroretinitis. Multifocal was the most common presentation, seen in about 95.6% of active toxoplasmosis simultaneously involving both the cases. T. gondii tends to affect the macula due to the high retina and the optic nerve is unusual, but was documented oxygen content owing to the end-arterial system of the retinal in an immunocompromised patient with human immuno- circulation. Retinochoroiditis is a more appropriate term for deficiency virus (HIV) infection. Differential diagnosis of acute inflammation, as the organism first lodges in the retina toxoplasmal lesions could be tuberculous granuloma, fungal followed by the choroid. endophthalmitis, sarcoid, syphilitic retinitis, cytomegalovirus The prevalence of toxoplasmosis in India shows a wide infection, intraocular lymphoma, and toxocariasis. variation. One study showed as high as 77% in women in the Histopathologically, the toxoplasmal lesion shows reproductive age-group.7 There is a report of this parasitic necrosis of the involved retina, with destruction of retinal infection among pregnant women in northeast India. In a architecture and underlying choroid. Since the parasite has study done by Borkakoty et al, the seroprevalence of T. gon- a propensity for attacking the neural tissue, the trophozoites dii infection was observed to be 44.6% and 36.8% among and the cysts are usually found in the superficial layers pregnant women with and without history of pregnancy of the retina within the areas of necrosis. The infiltrate wastage, respectively.8 A higher prevalence of T. gondii consists predominantly of lymphocytes, macrophages, and infection has been observed in women belonging to the epithelioid cells, with plasma cells found in the periphery lower socioeconomic class.8 It has also been observed that of the lesion.9,11,12 Cell-mediated immunity is said to be the the seroprevalence of T. gondii in humans in India is lower major defense mechanism against toxoplasmal infection. compared to their Western counterparts. This may be due to In patients with ocular toxoplasmosis, the cellular immune a preference for dogs as pets rather than cats in the Western responses appear to be directed predominantly against sur- population. face protein P22. However, some evidence also indicates The majority of reported cases of ocular toxoplasmosis that part of the disease may be mediated by autoimmune are congenital. The clinical manifestations of congenital mechanism directed against certain retinal antigens.12 ocular toxoplasmosis in infants include microphthalmia, The role of humoral response in toxoplasmosis remains enophthalmos, ptosis, nystagmus, choroidal coloboma, unclear. and strabismus.9,10 Posterior uveitis is the most common Ocular toxoplasmosis can be frequently diagnosed clini- manifestation, and presents as necrotizing retinitis usually cally on the basis of its characteristic retinochoroidal scar and adjacent to a larger atrophic retinochoroidal scar, which is inflammation. Serological testing confirms the clinical diag- often located in the macula in congenital cases. The critical nosis. There may be a history of eating undercooked or raw

2 submit your manuscript | www.dovepress.com Eye and Brain 2014:6 Dovepress Dovepress Zoonotic diseases in northeast India meat or being exposed to cats (source of acquired infection). the cysts. Any contact with cat feces should be avoided. The most common presentations of acquired toxoplasmosis Hand washing after touching uncooked meat and after con- are lymphadenopathy, fever, headache, malaise, pharyngitis, tact with cats or soil that could be contaminated with cat fatigue, and night sweats.13 feces should be practiced to avoid infection. Consumption In the case of congenital toxoplasmosis, inquiry about of raw eggs and nonpasteurized milk, particularly goat’s previous maternal abortion, birth history, history of ­seizures, milk, should be avoided. Fruits and vegetables should be etc, are important. Complete ocular examinations, including adequately washed before ingestion. Daily cleaning of the retinal evaluation, are also of paramount importance in these cat-litter box is also essential in order to prevent sporulation. cases. All patients are required to be seen by a physician for For females, only nonpregnant women should perform any remote lesion elsewhere in the body. this duty. Blood transfusions and organ transplants from Laboratory investigations include ELISA for toxoplas- seropositive individuals should be avoided if the recipient mosis (IgG, IgM, and IgA). This should show a positive is seronegative.9–12 titer from the current or any previous infection. However, Treatment should be considered if a lesion is at or near a negative titer on any dilution does not exclude the diagno- the optic disk (within two disk diameters), a lesion is within sis. IgM is found within 2–6 months of initial ­infection, after the temporal arcade, a lesion threatens the large retinal which only IgG remains positive. A 1:1 dilution should be vessel, a lesion has induced a substantial hemorrhage, done, as only a positive result is necessary in the setting of a lesion with an intense inflammatory reaction, extensive classical fundus findings. An HIV test should be considered chronic exudative lesions regardless of location, and in in any of the atypical cases or when the patient is a high- cases of severe vitreous haze, loss of two lines in visual risk candidate for AIDS. Anterior-chamber paracentesis acuity, persistence of inflammation for more than a month, for toxoplasmosis may be done where a polymerase chain congenital toxoplasmal retinochoroiditis in the first year of reaction (PCR) facility is available. This can be a useful tool life, newborn diagnosed as congenital toxoplasmosis regard- in the diagnosis of atypical toxoplasmosis cases, including less of the presence of ocular lesions, and any lesion in an the determination of local antibody production in aqueous immunocompromised host.9 humor. To demonstrate intraocular anti-T. gondii antibody Presently, newer drugs with fewer side effects are being production, total IgG amount and specific anti-T. gondii tried in ocular toxoplasmosis, but their long-term results IgG titers are determined with each serum and aqueous need to be further evaluated. Treatment options include a humor sample. Total IgG concentrations are measured by combination of pyrimethamine, sulfadiazine, and folinic acid nephelometry, and specific T. gondii IgG titers by highly with or without clindamycin. Trimethoprim and sulfame- sensitive agglutination tests. Recently, amplification of thoxazole combination is also another combination that is ribosomal ribonucleic acid gene of T. gondii from aqueous being tried in developing countries.9–11 Monotherapy with samples with PCR was found to be an important tool for the azithromycin and clindamycin is another good therapeutic diagnosis of toxoplasmosis.9 option, though recurrences have been seen with it.9–11 Oral The main aim of treatment is to stop the multiplication prednisolone is added to these regimens to counter the of tachyzoites during episodes of active retinochoroiditis. inflammatory reaction. Topical corticosteroids are used The disease is self-limited in immunocompetent patients. for anterior uveitis, but periocular injections are contrain- Mid-peripheral retinochoroiditis may not require ­treatment. dicated to avoid local immunosuppression and uncontrol- Some congenital cases with bilateral macular healed toxo- lable disease. Laser photocoagulation, cryotherapy, and plasmal scars require squint clinic evaluation, low-vision aid, vitrectomy are used as adjunctive treatment modalities. and regular follow-up. If there are complaints of headache Spiramycin is the treatment of choice in pregnant women or a suspicion of a neurological problem, skull X-ray or a with toxoplasmosis.9–11 computed tomography scan of brain is advised so as to look for any intracranial calcification, and further neurologist Cysticercosis consultation and follow-up may be required.9 The prevalence of in humans varies from 0.75% Measures for the prevention of toxoplasmosis are pri- to 1.0% in certain communities, particularly in rural areas, marily directed toward the prevention of primary infection. where there is more contact with pigs.1,14 Taeniasis is more Meat should be cooked up to 60°C for at least 15 minutes common in areas with poor hygiene. In India, neurocysticer- or frozen to below -20°C for at least 24 hours to destroy cosis is an important emerging disease of the central nervous

Eye and Brain 2014:6 submit your manuscript | www.dovepress.com 3 Dovepress Das et al Dovepress system, second to tuberculosis.1 Neurocysticercosis is also Patient: Clinic: SSN, Gowahati Gray: S1 24/JAN/09 Setting: General Depth: 4.0 0.0 15:49:48 emerging as one of the principal causes of epilepsy. The Patient ID: Eye: OS/left Operator: Gain: 63 Images: occurrence of Cysticercus cellulosae in muscles of pigs is Edge enh: off 10 MHZ 1,15,16 very well established, ranging from 3% to 26%. In India, Frozen little information on is available, due to a ban on the slaughter of cows and the majority of the population not consuming beef on religious grounds. Cysticercosis can also infect the eye. Intraocular cysticercosis management is somewhat different from the neurocysticercosis and orbital A-line or ocular adnexal cysticercosis.12 Humans are definitive hosts, and pigs are the interme- diate hosts of .17 In cysticercosis, humans become intermediate hosts by ingesting the eggs of T. solium from contaminated food and water. After enter- ing the intestinal wall, the embryo enters the bloodstream and can lodge in various organs, such as the central ner- vous system, eye, skeletal muscles, and subcutaneous 0 1 2 3 4 tissue.18,19 Autoinfections can also occur in some cases. Ocular involvement can be destructive, because cysticercus lesions gradually increase in size, leading to blindness in Figure 1 B-scan ultrasound showing cysticercus lesion with a scolex inside the cyst. 3–5 years. The death of the parasite causes the release of toxic substances, leading to intense inflammatory reactions by ­reattaching the retina subsequently.2 Often, granulomas and eye damage.17–19 Initial medical therapy of intraocular removed completely show atypical toxocaral lesions.2 Results cysticercosis with antihelminthic drugs like albendazole or of ELISAs performed on the vitreous samples are strongly praziquantel is not known to be very effective. Early surgi- positive. Photocoagulation and cryotherapy have also been cal removal of the parasite is the treatment of choice.17–19 tried in some cases to kill the organisms.2 Neurocysticercosis is also a worldwide problem, and thus it needs serious attention.17 Clinical, imaging (Figure 1), and pathological findings of cysticercosis patients presenting in Gnathostomiasis our center (a tertiary eye care center in Assam) have been Gnathostomiasis is a rare in humans, documented. Orbital cysticercosis is also seen in patients who become incidental hosts after the intake of under- from northeast India. cooked or raw meat of definitive hosts, such as cats, dogs

Toxocariasis infection is typically found in children. The average age of diagnosis is 7.5 years.2 T. canis is an ascarid that can only complete its life cycle in dogs. It is a ubiquitous parasite found worldwide, including India. Ocular involvement can present as retinal peripheral granuloma (Figure 2), posterior-pole granuloma, or endophthalmitis.2 Its systemic manifestations include fever, dry or hacking cough, hepatosplenomegaly, and neurological symptoms like convulsions. ELISA is the most reliable test, but is not commonly available in India. Intraocular manifestations respond well to steroids.2 Vitreoretinal surgery has also been suggested as an effective method by which the secondary effects of toxocariasis can be managed. Various authors have tried to address the retinal complications of this disorder Figure 2 Toxocara lesion in the left fundus.

4 submit your manuscript | www.dovepress.com Eye and Brain 2014:6 Dovepress Dovepress Zoonotic diseases in northeast India and wild animals.20 Second intermediate hosts may be the conjunctiva, and once each from the lower lid and the freshwater fish, chickens, snails, frogs, or paratenic hosts anterior chamber (Figure 4). like birds. After ingestion, the larvae cross the gastric and intestinal wall and migrate indiscriminately throughout the Hydatidosis 20 body. Clinical manifestations of gnathostomiasis occur or hydatidosis is an infection caused by the due to migration of parasitic larvae and host response to larval form of , and is a significant the toxins. We have come across two cases of intraocular public health problem. In India, there is an alarming increase gnathostomiasis in our center, one of which was in the of this infection, mostly in north India.13 The presence of stray vitreous cavity, while the other was seen in the iris tissue. dogs and dead carcasses plays an important role in the trans- The first was published, and in both the cases the live worm mission of this disease in our country.1,33 However, it has been 20 was retrieved (Figure 3). observed that ocular involvement of hydatidosis is not very Gnathostomiasis is most prevalent in Southeast Asia and common in this part of the country. Nicholson et al reported Latin America, with an increasing global trend. Travel patterns, seven cases of hydatid cysts of the orbit.34 We have also seen food habits, and aquaculture for tourism involving hunting and and documented cases of hydatid disease in the eye and ocular fishing may be responsible for this rise in the global incidence. adnexa. Three cases of orbital hydatidosis have been seen in Ocular gnathostomiasis may involve the eyelids, conjunctiva, our center. An interesting observation in the histopathology 20–22 cornea, anterior chamber, uvea, or vitreous. The com- of the cyst wall was made. It showed multiple pores in the 20,23 monest ocular clinical manifestation is anterior uveitis. laminated structures of the cyst wall. We believe these pores Consumption of smoked or undercooked fish may have to be the route of passage of fluid in and out of the cyst. contributed to the occurrence of the disease in this particular region of India.20 Ocular involvement of thelaziasis infection is rare. The first Dirofilariasis human case of callipaeda infection was reported from Dirofilariasis is a zoonotic disease seen in different parts Vietnam.35 This is a zoonotic parasite in the eyes, of the world.24–26 The worm may get lodged in various tis- as implied by its name “Oriental eye worm” or “eye worm”.35 sues of the human body, including the eye and ocular adn- It was reported for the first time in a dog from Pakistan in exa.24–32 There may be deep-seated infection, such as in the 1910. Subsequently, thelaziasis cases have been reported lungs, where early and proper diagnosis can save a patient from the People’s Republic of , , , India, from major complications.24–27 Dirofilariasis infections ­, , , South , the , Russia, are often reported in European, Mediterranean, and Asian ­, , Myanmar, and .36 The adult worm countries.24–27 There are few reports of ocular dirofilariasis is parasitic in the conjunctival sac of a host, and produces larvae from India.30 We have had five cases of unpublished ocular ­continuously. When lick the tear in the eye of the final dirofilariasis. In three cases, the worm was extracted from

Figure 3 Parasite ( spp.) in the iris of the right eye. Figure 4 Live parasite in the anterior chamber of the right eye ().

Eye and Brain 2014:6 submit your manuscript | www.dovepress.com 5 Dovepress Das et al Dovepress host, such as humans, the larvae enter the conjunctival sac and become adult in 1 month. Symptoms of T. callipaeda infection include excessive watering, visual impairment, ulcers, and scar- ring of the cornea.37,38 We have also seen cases of ocular adnexal thelaziasis infection (Figures 5 and 6) in our center.

Amebiasis and giardiasis Human infection due to Entamoeba histolytica has been reported in India. A study showed many animals to be potential reservoirs of infection. Although it mainly affects the gastro- intestinal tract, intraocular inflammatory disease has also been associated with it.39 It is diagnosed by identifying the cysts and the trophozoites. Acanthamoeba spp. are also known to affect the eyes, particularly corneas. Giardiasis intestinalis is com- mon in children and occasionally in HIV-infected individuals. Ocular manifestations of giardiasis include iridocyclitis,40 chorioretinitis,41 and “salt and pepper” fundus.41 Diagnosis of giardiasis can be made from the stool sample, while in some cases jejunal biopsy may be required. Quinacrine hydrochloride or metronidazole is effective for the treatment for giardiasis.

Larva migrans, diffuse unilateral subacute neuroretinitis More than 200 million people are affected by in India.1,2 Both and visceral larva

Figure 6 Scanning electron microscopy ([A] 1400× and [B] 1900×) showing the proximal part of Thelazia.

migrans have been reported throughout the country. They are caused by and A. braziliense. However, A. ceylanicum was detected in dogs living among the tea-growing community. This may lead to an endemicity of the parasite in northeast India.1,2,42 A rare eye condition called diffuse unilateral subacute neuroretinitis has been described, which is very rarely seen in the retina and choroid. A. caninum and procyonis (a nematode found in raccoon) were found to be associated with it.43

Cryptosporidiosis Cryptosporidiosis has been reported worldwide. Cryptosporidium parvum, which is associated with diar- rhea in ­children, has also been reported from various parts of India.44,45 Ocular manifestation, which is rare, occurs in the form of . It is seen in urban slum areas in patients with diarrhea. It is also an opportunistic infection

Figure 5 Thelazia retrieved from the conjunctival sac. in HIV-infected individuals.

6 submit your manuscript | www.dovepress.com Eye and Brain 2014:6 Dovepress Dovepress Zoonotic diseases in northeast India

9. Jain L, Das D, Bhattacharjee H, Jain G. Ocular toxoplasmosis. Delhi J Conclusion Ophthalmol. 2009;15:19–23. There are various factors that favor zoonoses in northeastern 10. De Jong PT. Ocular toxoplasmosis: common and rare symptoms and states of India. Increased vector populations, poverty, food signs. Int Ophthalmol. 1989;13:391–397. habits, large numbers of stray animals, poor personal hygiene, 11. Jabs DA. Ocular toxoplasmosis. Int Ophthalmol Clin. 1990;30: 264–270. and lack of awareness of the diseases are some of the factors 12. Nussenblatt RB, Mittal KK, Fuhrman S, Sharma SD, Palestine AG. responsible. It has been observed that certain zoonotic diseases Lymphocyte proliferative responses of patients with ocular toxoplas- mosis to parasite and retinal antigens. Am J Ophthalmol. 1989;107: are showing a rising trend, such as toxoplasmosis and gnathos- 632–641. tomiasis. A systematic study on zoonoses is required to make 13. Zimmerman LE. Ocular pathology of toxoplasmosis. Surv Ophthalmol. the final comment on these observations. Health education, 1961;6:832–856. 14. Singh GS, Prabhakar S, Cho SY, et al. Taenia solium taeniasis and cysticer- vector control, control of animal movements, control over road- cosis in Asia. In: Singh GS, Prabhakar S, editors. Taenia solium Cysticer- side slaughter of animals, safe water supply, food hygiene, and cosis: From Basic to Clinical Science. Oxford: CABI; 2002:111–128. 15. D’Souza P. Studies on porcine cysticercosis with special reference to socioeconomic development are essential in order to prevent serodiagnosis. J Vet Parasitol. 1998;12:64. these zoonotic diseases. Proper diagnosis in time may even 16. Prasad KN, Chawla S, Jain D, et al. Human and porcine Taenia solium save vision and lives. Therefore, proper coordination between in rural north India. Trans R Soc Trop Med Hyg. 2002;96:515–516. 17. Das D, Deka S, Islam S, et al. 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